A reduction in floral resource abundance and diversity is generally observed in agro-ecosystems, along with widespread exposure to pesticides. Therefore, a better understanding on how the availability and quality of pollen diets can modulate honeybee sensitivity to pesticides is required. For that purpose, we evaluated the toxicity of acute exposure and chronic exposures to field realistic and higher concentrations of azoxystrobin (fungicide) and sulfoxaflor (insecticide) in honeybees provided with pollen diets of differing qualities (named S and BQ pollens). We found that pollen intake reduced the toxicity of the acute doses of pesticides. Contrary to azoxystrobin, chronic exposures to sulfoxaflor increased by 1.5- to 12-fold bee mortality, which was reduced by pollen intake. Most importantly, the risk of death upon exposure to a high concentration of sulfoxaflor was significantly lower for the S pollen diet when compared with the BQ pollen diet. This reduced pesticide toxicity was associated with a higher gene expression of vitellogenin, a glycoprotein that promotes bee longevity, a faster sulfoxaflor metabolization and a lower concentration of the phytochemical p -coumaric acid, known to upregulate detoxification enzymes. Thus, our study revealed that pollen quality can influence the ability of bees to metabolize pesticides and withstand their detrimental effects, providing another strong argument for the restoration of suitable foraging habitat.

With 2,000 species currently recorded in Europe, bees are a highly diversified and efficient group of pollinating insects. They obtain their nutrients from nectar and pollen of flowers. However, the chemical composition of these resources, especially of pollen (e.g., protein, lipid, amino acids, fatty acids, or sterol content), is highly variable among plant species. While it is well-known that bees show interspecific variation in their floral choices, there is a lack of information on the nutritional requirements of different bee species. We therefore developed original experiments in laboratory conditions to evaluate the interspecific variations in bee nutritional requirements. We analyzed the chemical content of eight pollen blends, different in terms of protein, lipid, amino acids, and sterols total concentration and profiles. Each pollen blend was provided to four different bee model species: honey bees (Apis mellifera), bumblebees (Bombus terrestris), mason bees (Osmia bicornis and Osmia cornuta). For each species, specific protocols were used to monitor their development (e.g., weight, timing, survival) and resource collection. Overall, we found that the nutritional requirements across those species are different, and that a low-quality diet for one species is not necessarily low-quality for another one. While honey bees are negatively impacted by diets with a high protein content (~40%), bumblebees and mason bees develop normally on these diets but struggle on diets with a low total amino acid and sterol content, specifically with low concentrations of 24-methylenecholesterol and β-sitosterol. Overall, our study supports the need of conserving and/or introducing plant diversity into managed ecosystems to meet the natural nutritional preferences of bees at species and community level.

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Highlights There is a gap between new evidence of pesticide toxicity in honeybees and regulatory toxicological bioassays  Current endpoints should be complemented with behavioral and reproductive endpoints  We review such endpoints and discuss their possible use in pesticide risk assessment  There is a need to translate toxicological research studies into regulatory test methods

Toxicological studies in honeybees have long shown that a single pesticide dose or concentration does not necessarily induce a single response. Inter-individual differences in pesticide sensitivity and/or the level of exposure (e.g. ingestion of pesticide-contaminated matrices) may explain this variability in risk posed by a pesticide. Therefore, to better inform pesticide risk assessment for honeybees, we studied the risk posed by pesticides to two behavioral castes, nurse and forager bees, which are largely represented within colonies and which exhibit large differences in their physiological backgrounds. For that purpose, we determined the sensitivity of nurses and foragers to azoxystrobin (fungicide) and sulfoxaflor (insecticide) upon acute or chronic exposure. Azoxystrobin was found to be weakly toxic to both types of bees. However, foragers were more sensitive to sulfoxaflor than nurses upon acute and chronic exposure. This phenomenon was not explained by better sulfoxaflor metabolization in nurses, but rather by differences in body weight (nurses being 1.6 times heavier than foragers). Foragers consistently consumed more sugar syrup than nurses, and this increased consumption was even more pronounced with pesticide-contaminated syrup (at specific concentrations). Altogether, the stronger susceptibility and exposure of foragers to sulfoxaflor contributed to increases of 2 and 10-fold for the acute and chronic Risk Quotients, respectively, compared to nurses. In conclusion, to increase the safety margin and avoid an under-estimation of the risk posed by insecticides to honeybees, we recommend systematically including forager bees in regulatory tests.

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